Foraging behaviour influences the outcome of predator–predator interactions

Abstract.  1. Interactions among predators may influence the total efficiency of a predator complex. The effect of intra- and interspecific interactions of the generalist predators Orthotylus marginalis (Heteroptera: Miridae) and Anthocoris nemorum (Heteroptera: Anthocoridae) was investigated in a laboratory experiment. Outcomes of the interactions were determined by comparing predation rates on eggs and larvae of the blue willow beetle Phratora vulgatissima of single individuals with those of two individuals of the same or different species.
2. A non-additive, antagonistic effect on predation rates due to intraspecific interactions was found between individuals of A. nemorum . No such effect was found in O. marginalis . These results are as expected as a consequence of differences in behaviour of the two predator species: A. nemorum is a much more active and mobile predator than O. marginalis .
3. Contrary to expectation, interspecific interactions between A. nemorum and O. marginalis did not affect the total predation rate.
4. An observation from the field corroborated the results obtained in the laboratory study; there was no negative relationship between the densities of the two predator species, indicating that the two species do not interact negatively in the field at their natural densities.
5. It is concluded that the additive effect of multiple predator species is of potential value in biological control.     

Inbreeding alters a plant-predispersal seed predator interaction

The effect of inbreeding on genetic diversity is expected to decrease plant defences or vigour-related traits that, in turn, can modify the pattern of attack by herbivores. The selective damage caused by herbivores can produce variable fitness costs between inbred and outcrossed progenies influencing the evolution of a species’ plant mating system. By exposing inbred and outcrossed plants to natural conditions of seed predation, we assessed whether inbreeding increases weevil incidence and infestation, and how weevil seed predation affects the fitness of inbred and outcrossed progeny. To test if inbreeding affected the host’s plant quality, we weighed the biomass of weevils developed in inbred and outcrossed progenies. An additional experiment was carried out to examine whether weevils preferentially attack vigorous plants regardless from the level of inbreeding. The average value of leaf size was 21% larger in outcrossed plants than in inbred plants. Likewise, weevil incidence and infestation were 13 and 40%, respectively, higher on outcrossed plants relative to their inbred counterparts. However, the relative impact of seed predation was significantly lower in outcrossed progeny than in inbred progeny. In contrast, inbreeding did not alter host plant quality and weevils developed in inbred and outcrossed plants had a similar biomass. Variations in fruit number were consistently associated with the infestation level in both experiments, whereas leaf size only predicted the number of weevils in one experiment, suggesting that fruit number is the most influential vigour-related characteristic of a weevil attack. These findings indicate that the costs of inbreeding of the interaction D. stramonium-T. soror were higher for inbred plants than for outcrossed plants. The interaction between seed predation and inbreeding depression could prevent the fixation of selfing as a unique reproductive strategy in D. stramonium.     

Structure in plant–animal interaction assemblages

We present a comprehensive approach to detect pattern in assemblages of plant and animal species linked by interactions such as pollination, frugivory or herbivory. Simple structural models produce gradient, compartmented or nested patterns of interaction; intermediate patterns between a gradient and compartments are possible, and nesting within compartments produces a combined model. Interaction patterns can be visualized and analyzed either as matrices, as bipartite networks or as multivariate sets through correspondence analysis. We argue that differences among patterns represent outcomes of distinct evolutionary and ecological processes in these highly diversified assemblages. Instead of choosing one model a priori, assemblages should be probed for a suite of patterns. A plant–pollinator assemblage exemplifies a simple nested pattern, whereas a plant–herbivore assemblage illustrates a compound pattern with nested structures within compartments. Compartmentation should reflect coevolutionary histories and constraints, whereas differences in species abundance or dispersal may generate nestedness.     

Habitat context influences predator interference interactions and the strength of resource partitioning

Despite increasing evidence that habitat structure can shape predator–prey interactions, few studies have examined the impact of habitat context on interactions among multiple predators and the consequences for combined foraging rates. We investigated the individual and combined effects of stone crabs (Menippe mercenaria) and knobbed whelks (Busycon carica) when foraging on two common bivalves, the hard clam (Mercenaria mercenaria) and the ribbed mussel (Geukensia demissa) in oyster reef and sand flat habitats. Because these species co-occur across these and other estuarine habitats of varying physical complexity, this system is ideal for examining how habitat context influences foraging rates and the generality of predator interactions. Consistent with results from previous studies, consumption rates of each predator in isolation from the other were higher in the sand flat than in the more structurally complex oyster reef habitat. However, consumption by the two predators when combined surprisingly did not differ between the two habitats. This counterintuitive result probably stems from the influence of habitat structure on predator–predator interactions. In the sand-flat habitat, whelks significantly reduced their consumption of their less preferred prey when crabs were present. However, the structurally more complex oyster reef habitat appeared to reduce interference interactions among predators, such that consumption rates when the predators co-occurred did not differ from predation rates when alone. In addition, both habitat context and predator–predator interactions increased resource partitioning by strengthening predator dietary selectivity. Thus, an understanding of how habitat characteristics such as physical complexity influence interactions among predators may be critical to predicting the effects of modifying predator populations on their shared prey.     

A seed predator drives the evolution of a seed dispersal mutualism

Although antagonists are hypothesized to impede the evolution of mutualisms, they may simultaneously exert selection favouring the evolution of alternative mutualistic interactions. We found that increases in limber pine (Pinus flexilis) seed defences arising from selection exerted by a pre-dispersal seed predator (red squirrel Tamiasciurus hudsonicus) reduced the efficacy of limber pine's primary seed disperser (Clark's nutcracker Nucifraga columbiana) while enhancing seed dispersal by ground-foraging scatter-hoarding rodents (Peromyscus). Thus, there is a shift from relying on primary seed dispersal by birds in areas without red squirrels, to an increasing reliance on secondary seed dispersal by scatter-hoarding rodents in areas with red squirrels. Seed predators can therefore drive the evolution of seed defences, which in turn favour alternative seed dispersal mutualisms that lead to major changes in the mode of seed dispersal. Given that adaptive evolution in response to antagonists frequently impedes one kind of mutualistic interaction, the evolution of alternative mutualistic interactions may be a common by-product.     

Environmental context drives seed predator-mediated selection on a floral display trait

Linking trait selection to environmental context is necessary to move beyond the simple recognition that selection is spatially variable and to understand what ultimately drives this variation. Natural selection acts through differences among individuals in lifetime fitness and information about effects on fitness components is therefore often not sufficient to gain such an understanding. We investigated how environmental context influenced intensity of seed predation, flower abortion and selection on floral display traits in 44–52 populations of the perennial herb Primula veris over 2 years. Phenotypic selection on both inflorescence height and flower number varied among populations and was mediated partly by pre-dispersal seed predation and flower abortion in one of the years. Among-population variation in selection on inflorescence height, but not flower number, was linked to variation in canopy cover via its effects on seed predation. Lifetime fitness was less sensitive to seed predator damage in shaded environments but estimates of selection based on lifetime fitness agreed qualitatively with those based on seed output. Our results demonstrate that seed predators constitute an important link between environmental conditions and trait evolution in plants, and that selection on plant traits by seed predators can depend on environmental context.     

Interactions between a pollinating seed predator and its host plant: the role of environmental context within a population

Plant–insect interactions often are important for plant reproduction, but the outcome of these interactions may vary with environmental context. Pollinating seed predators have positive and negative effects on host plant reproduction, and the interaction outcome is predicted to vary with density or abundance of the partners. We studied the interaction between Silene stellata, an herbaceous perennial, and Hadena ectypa, its specialized pollinating seed predator. Silene stellata is only facultatively dependent upon H. ectypa for pollination because other nocturnal moth co‐pollinators are equally effective at pollen transfer. We hypothesized that for plants without conspecific neighbors, H. ectypa would have higher visitation rates compared to co‐pollinators, and the plants would experience lower levels of H. ectypa pollen deposition. We predicted similar oviposition throughout the study site but greater H. ectypa predation in the area without conspecific neighbors compared to plants embedded in a naturally high density area. We found that H. ectypa had consistently higher visitation than moth co‐pollinators in all host plant contexts. However, H. ectypa pollinator importance declined in areas with low conspecific density because of reduced pollen deposition, resulting in lower seed set. Conversely, oviposition was similar across the study site independent of host plant density. Greater likelihood of very high fruit predation combined with lower pollination by H. ectypa resulted in reduced S. stellata female reproductive success in areas with low conspecific density. Our results demonstrate local context dependency of the outcomes of pollinating seed predator interactions with conspecific host plant density within a population.     

Bird dispersal of the larval stage of a seed predator

Multiflora rose seeds containing larvae of the phytophagous wasp Megastigmus aculeatus nigroflavus were fed to a caged mockingbird (Mimus polyglottos). Ninety percent of the seeds were recovered from the bird's feces, and there was no significant difference in subsequent emergence of the wasps from these seeds when compared to controls. This study indicates the dispersal of seed-feeding hymenoptera by avian frugivores may be a widespread and significant phenomenon.     

The context dependence of non‐consumptive predator effects

Non‐consumptive predator effects (NCEs) are now widely recognised for their capacity to shape ecosystem structure and function. Yet, forecasting the propagation of these predator‐induced trait changes through particular communities remains a challenge. Accordingly, focusing on plasticity in prey anti‐predator behaviours, we conceptualise the multi‐stage process by which predators trigger direct and indirect NCEs, review and distil potential drivers of contingencies into three key categories (properties of the prey, predator and setting), and then provide a general framework for predicting both the nature and strength of direct NCEs. Our review underscores the myriad factors that can generate NCE contingencies while guiding how research might better anticipate and account for them. Moreover, our synthesis highlights the value of mapping both habitat domains and prey‐specific patterns of evasion success (‘evasion landscapes’) as the basis for predicting how direct NCEs are likely to manifest in any particular community. Looking ahead, we highlight two key knowledge gaps that continue to impede a comprehensive understanding of non‐consumptive predator–prey interactions and their ecosystem consequences; namely, insufficient empirical exploration of (1) context‐dependent indirect NCEs and (2) the ways in which direct and indirect NCEs are shaped interactively by multiple drivers of context dependence.     

Exploring the impact of a non-native seed predator on the seed germination of its non-native host

Biological Invasions - Novel interactions between introduced and native species commonly occur and can even be predicted from existing native interactions in a certain area. However, novel...     

Trichomes of the seed fern Blanzyopteris praedentata: implications for plant–insect interactions in the Late Carboniferous

The fronds and compound tendrils of the Stephanian (Late Carboniferous) seed fern Blanzyopteris praedentata possess several types of trichomes, two of which may, based on their morphology, have functioned as deterrents against herbivores. Bands of upwardly curved trichomes, occurring on the adaxial surfaces of tendrils, frond- and pinna rachides, are also known from extant plants, where they create mechanical obstacles. Other trichomes that are glandular occur on most parts of the foliage and tendrils and represent a different form of defence mechanism. These trichomes apparently possessed a touch-sensitive mechanism that opened the secretory cell when touched. They are interpreted as functionally similar to the so-called 'explosive' trichomes of certain extant Cucurbitaceae and Solanaceae. Studies of living Oleander aphids ( Aphis nerii ) on Sicana odorifera (Cucurbitaceae) demonstrate the effectiveness of the physical component of this defence. When touched and ruptured by an aphid, the trichomes of S. odorifera rapidly release a sticky exudate, which adheres to the animal's legs; the accumulation of exudate on the legs eventually impedes the aphid. Based on these studies, hypotheses are presented on the types of animals that might have been deterred by the glandular trichomes of B. praedentata in the Late Carboniferous.  © 2003 The Linnean Society of London, Botanical Journal of the Linnean Society , 2003, 141 , 133–149.     

The effects of seed availability on habitat use by a specialist seed predator

Space-use patterns of seed predators are strongly affected by spatiotemporal variation in the abundance of different tree seeds, their major food source. However, most studies have measured relationships between overall food availability and space use, and there are few cases where effects of different food resources have been explored. We studied the effects of two food resources, Norway spruce and silver fir seeds, on space and habitat use in red squirrel in a subalpine conifer forest from 2000 to 2006. Fir seeds disperse in the autumn of the year they are produced, spruce the following spring. We estimated spruce and fir seed availability within individual home ranges and monitored home-range size using radiotelemetry. Males had larger home ranges than females and the sexes responded differently to variation in food and density. Spruce seed availability negatively affected home-range and core-area sizes of males in spring–summer. Space use was not affected by fir seed availability. Squirrels positively selected spruce for foraging and spruce was always preferred over fir. Our results showed that spruce, but not fir, affected space and habitat use of squirrels, suggesting they do not behaviourally respond to early seed dispersal in fir.     

An interaction between a specialized seed predator moth and its dioecious host plant shifting from parasitism to mutualism

Seed predator/pollinator and host plant interactions, which may be considered as antagonistic, have the potential to provide good model systems for the study of the early stages of evolution towards mutualism. I describe a relationship between a seed predator, the geometrid moth Perizoma affinitatum , and the dioecious plant Silene dioica . The moth is an obligate seed predator on its host plant. The searching and ovipositing behaviour of the female moths, number of eggs deposited per flower, the pollinating ability of the moths and the seed consumption by the larvae are described as different parameters and studied in two Finnish coastal populations. A high pollinating ability and limited seed consumption by the predator was found and discussed in relation to fitness models of P. affinitatum and S. dioica . In a mutualistic relationship there must be a balance between the costs and benefits so that the seed production by the moths is larger than the seed consumption by the larvae, given a net seed output larger than zero. The data of the parameters included in a seed production/consumption model give a positive seed output when the proportion of S. dioica flowers pollinated by other non-predating insects is less than 60%. Accordingly, even if P. affinitatum would become the exclusive pollinator it would not endanger the survival of the host plant and both partners would benefit from this interaction. Limited seed consumption, high pollinating ability and host specificity as seen in the P. affinitatum and S. dioica interaction are considered to have been important pre-existing qualities in the evolution of the obligate mutualisms between yucca and yucca moths and fig and fig wasps. In isolated serpentine populations where the gene flow is restricted and co-pollinators are rare the interaction between P. affinitatum and S. dioica has the potential to shift from parasitism to mutualism.     

A local accumulation of the Ralstonia solanacearum PopA protein in transgenic tobacco renders a compatible plant–pathogen interaction incompatible

Plants activate disease resistance responses when they recognize pathogen-derived molecules (elicitors). Frequently, recognition results in a hypersensitive response (HR), which is characterized by local host cell death at the infection site. Here we describe a genetic engineering approach to generate an HR in plants, whether or not an invading micro-organism produces a recognized elicitor. To that aim we created transgenic tobacco plants in which the pathogen-inducible promoter of the hsr203J gene from tobacco controls the expression of the popA elicitor gene from Ralstonia solanacearum. Because PopA itself also induces the hsr203J promoter, transgenic plants rapidly accumulate the bacterial elicitor in the pathogen infection sites. The elicitor becomes converted in plant tissues into its fully active derivatives PopA1-PopA3, showing that the previously observed processing events are not dependent on the bacterial type III secretion system. The outcome of induced PopA accumulation is a localized HR and a high degree of resistance of the transgenic plants to an oomycete pathogen. The system is functional in hybrids between different tobacco varieties, and we show that the engineered resistance, but not the associated cell death, is dependent on the salicylic acid signalling cascade. Although the approach is powerful in generating oomycete resistance, the induced HR might affect plant health. Its application thus requires a careful selection of individual transgenic lines and trials with various pathogens.     

The context of tetanus toxoid application influences the outcome of antigen-specific and self-directed humoral immune response

Results are presented concerning our attempts to create a suitable model system for studying the connection between microbial antigen (micAg), autoimmunity and autoimmune disease on the basis of hyper-immunization and application of micAg in different contexts. Our research was focused on tetanus toxoid (TTd) as a model micAg. Non-pretreated and complete Freund's adjuvant pretreated BALB/c mice were immunized with high doses of TTd mixed with glycerol or aluminum hydroxide as adjuvants. The main aims of the experiments were to evaluate the properties of induced humoral immune responses, evaluate the pathological potential of induced immune responses and determine possible correlations between the properties of a humoral immune response and its pathological potential. The production of TTd-specific and self-reactive β₂-glycoprotein I (β₂-GP I)-specific antibodies (Abs) was detected in all groups but with specific, context-related properties. Analysis of pregnancy-related pathology (anti-β₂-GP I Abs-associated) showed differences in the pathological potential of the induced immune response. It was demonstrated that severity of pathology is positively correlated to the abundance of IgG that recognizes β₂-GP I adsorbed onto phosphatidylserine, and to IgG affinity. Furthermore, it was demonstrated that molecular mimicry, which results in generation of anti-β₂-GP I Abs upon TTd immunization, is necessary but not sufficient for the development of pregnancy-related pathology.